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Ceratomyxa mennani n. sp. (Myxosporea: Bivalvulida) parasitizing the gallbladder of the dusky grouper Epinephelus marginatus (Serranidae) from Tunisian waters

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Abstract

Ceratomyxa mennani n. sp. is a new coelozoic Ceratomyxa species found in the gallbladder of Epinephelus marginatus from the Gulf of Tunis, Tunisia. Mature plasmodia were disporic, ovoid in shape measuring 9–12 μm in width and 11–14 μm in length. Mature myxospores were slightly crescent-shaped with almost straight posterior margin, measuring 5.8 ± 0.2 (5.4–6.1) μm in length and 12.7 ± 0.3 (11.9–13.0) μm in thickness. The two valves were unequal with rounded ends. Polar capsules were spherical, equal in size with 2.1 ± 0.2 (1.9–2.6) μm in diameter. The binucleated sporoplasm filled the entire cavity of the myxospore. Molecular analysis of SSU rDNA sequences indicated that C. mennani n. sp. was distinct from all other Ceratomyxa sequences in GenBank. Phylogenetic analysis revealed that C. mennani n. sp. clustered with Ceratomyxa species infecting Epinephelinae fishes. Seasonal prevalence of infection over one year was significantly higher in winter and the lowest in autumn. This is the third report of Ceratomyxa species infecting the gallbladder of Epinephelus marginatus from Tunisia and the first study to include molecular data.

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References

  • Abdel-Baki AA, Al-Qahtani HA, Al-Quraishy SA, Mansour L (2017) Ceratomyxa azevedoi n. sp. (Myxozoa: Myxosporea) parasitizing the gallbladder of Lutjanus ehrenbergii in the Arabian Gulf. Parasitol Res 116(10):2757–2763

    PubMed  Google Scholar 

  • Abdel-Baki AA, Mansour L, Al-Qahtani HA, Al Omar SY, Al-Quraishy SA (2015) Morphology, seasonality and phylogenetic relationships of Ceratomyxa husseini n. sp. from the gall-bladder of Cephalopholis hemistiktos (Ruppell) (Perciformes: Serranidae) in the Arabian Gulf off Saudi Arabia. Syst Parasitol 91:91–99

    PubMed  Google Scholar 

  • Alama-Bermejo G, Raga JA, Holzer AS (2011) Host–parasite relationship of Ceratomyxa puntazzi n. sp. (Myxozoa: Myxosporea) and sharpsnout seabream Diplodus puntazzo (Walbaum, 1792) from the Mediterranean with first data on ceratomyxid host specificity in sparids. Vet Parasitol 182:181–192

    CAS  PubMed  Google Scholar 

  • Alama-Bermejo G, Šíma R, Raga JA, Holzer AS (2013) Understanding myxozoan infection dynamics in the sea: seasonality and transmission of Ceratomyxa puntazzi. Int J Parasitol 43(9):771–780

    PubMed  Google Scholar 

  • Andrade AB, Machado LF, Hostim-Silva M, Barreiros JP (2003) Reproductive biology of the dusky grouper Epinephelus marginatus ( Lowe, 1834). Braz Arch Biol Technol 46(3):373–381

    Google Scholar 

  • Antonio DB, Andree K, McDowell TS, Hedrick RP (1998) Detection of Myxobolus cerebralis in rainbow trout and oligochaete tissues by using a nonradioactive in situ hybridization (ISH) protocol. J Aquat Anim Health 10(4):338–347

    Google Scholar 

  • Antonio DB, El-Matbouli M, Hedrick RP (1999) Detection of early developmental stages of Myxobolus cerebralis in fish and tubificid oligochaete hosts by in situ hybridization. Parasitol Res 85(11):942–944

    CAS  PubMed  Google Scholar 

  • Barta JR, Martin DS, Liberator PA, Dshkevicz M et al (1997) Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. J Parasitol 83:262–271

    CAS  PubMed  Google Scholar 

  • Condini MV, Hoeinghaus DJ, Garcia AM (2015) Trophic ecology of dusky grouper Epinephelus marginatus (Actinopterygii, Epinephelidae) in littoral and neritic habitats of southern Brazil as elucidated by stomach contents and stable isotope analyses. Hydrobiologia 743:109–125

    Google Scholar 

  • Condini MV, García-Charton JA, Garcia AM (2018) A review of the biology, ecology, behavior and conservation status of the dusky grouper, Epinephelus marginatus (Lowe 1834). Rev Fish Biol Fish 28(2):301–330

    Google Scholar 

  • Craig MT, Sadovy de Mitcheson YJ, Heemstra PC (2011) Groupers of the world: a field and market guide, Boca Raton

  • Eiras JC (2006) Synopsis of the species of the genus Ceratomyxa Thélohan, 1892 (Myxozoa, Myxosporea, Ceratomyxidae). Syst Parasitol 65:49–71

    CAS  PubMed  Google Scholar 

  • Eiras JC, Cruz C, Saraiva A (2018) Synopsis of the species of Ceratomyxa Thélohan, 1892 (Cnidaria, Myxosporea, Ceratomyxidae) described between 2007 and 2017. Syst Parasitol 95(5):427–446. https://doi.org/10.1007/s11230-018-9791-3

  • El-Matbouli M, Hoffmann RW (1989) Experimental trans-mission of two Myxobolus spp. develo** bisporogeny via tubificid worms. Parasitol Res 75:461–464

    CAS  PubMed  Google Scholar 

  • El-Matbouli M, McDowell TS, Antonio DB, Andree KB, Hedrick RP (1999) Effect of water temperature on the development, release and survival of the triactinomyxon stage of Myxobolus cerebralis in its oligochaete host. Int J Parasitol 29:627–641

    CAS  PubMed  Google Scholar 

  • Fiala I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol 36:1521–1534. https://doi.org/10.1016/j.ijpara.2006.06.016

    Article  CAS  PubMed  Google Scholar 

  • Figueiredo IL, Menezes NA (1980) Manual de peixes marinhos do sudeste do Brasil. III. Teleostei (2). São Paulo, Museu de Zoologia da Universidade de São Paulo

  • Garbouj M, Rangel LF, Castro R, Hmissi J, Santos MJ, Bahri S (2016) Morphological description and phylogeny of Ceratomyxa scorpaeni n. sp. (Myxosporea: Ceratomyxidae) infecting the gallbladder of Scorpaena porcus (L.) (Scorpaeniformes: Scorpaenidae) from the Bay of Bizerte in Tunisia. Parasitol Res 115(12):4495–4502

    PubMed  Google Scholar 

  • Gunter NL, Adlard RD (2008) Bivalvulidan (Myxozoa: Myxosporea) parasites of damselfishes with description of twelve novel species from Australia’s Great Barrier Reef. Parasitology 135:1165–1178

    CAS  PubMed  Google Scholar 

  • Gunter NL, Adlard RD (2009) Seven new species of Ceratomyxa from the gall bladders of serranids from the Great Barrier Reef, Australia. Syst Parasitol 73:1–11

    PubMed  Google Scholar 

  • Gunter NL, Whipps CM, Adlard RD (2009) Ceratomyxa (Myxozoa: Bivalvulida): robust taxon or genus of convenience? Int J Parasitol 39:1395–1405

    PubMed  Google Scholar 

  • Hallett SL, Diamant A (2001) Ultrastructure and small-subunit ribosomal DNA sequence of Henneguya lesteri n.sp. (Myxosporea), a parasite of sand whiting Sillago analis (Sillaginidae) from the coast of Queensland, Australia. Dis Aquat Org 46:197–212. https://doi.org/10.3354/dao046197

    Article  CAS  PubMed  Google Scholar 

  • Hedrick RP, McDowell TS, Mukkatira K, MacConnell E, Petri B (2008) Effects of freezing, drying, ultraviolet irradiation, chlorine, and quaternary ammonium treatments on the infectivity of myxospores of Myxobolus cerebralis for Tubifex tubifex. J Aquat Anim Health 20:116–125

    PubMed  Google Scholar 

  • Heemstra PC, Randall JE (1993) FAO Species Catalogue. Vol. 16. Groupers of the world (family Serranidae, subfamily Epinephelinae). An annotated and illustrated catalogue of the grouper, rockcod, hind, coral grouper and lyretail species known to date. Rome: FAO. FAO Fish. Synop 125(16):382

  • Heiniger H, Gunter NL, Adlard RD (2008) Relationships between four novel ceratomyxid parasites from the gall bladders of labrid fishes from Heron Island, Queensland, Australia. Parasitol Int 57(2):158–165

    CAS  PubMed  Google Scholar 

  • Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411–453

    CAS  PubMed  Google Scholar 

  • Hogg ID, Williams DD (1996) Response of stream invertebrates to a global-warming thermal regime: an ecosystem-level manipulation. Ecology 77(2):395–407

    Google Scholar 

  • Hogg ID, Williams DD, Eadie JM, Butt SA (1995) The consequences of global warming for stream invertebrates: a field simulation. J Therm Biol 20:199–206

    Google Scholar 

  • Kallert DM, El-Matbouli M (2008) Differences in viability and reactivity of actinospores of three myxozoan species upon ageing. Folia Parasitol 55:105–110

    PubMed  Google Scholar 

  • Køie M, Karlsbakk E, Nylund A (2008) The marine herring myxozoan Ceratomyxa auerbachi (Myxozoa: Ceratomyxidae) uses Chone infundibuliformis (Annelida: Polychaeta: Sabellidae) as invertebrate host. Folia Parasitol 55(2):100–104

    PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    CAS  PubMed  Google Scholar 

  • Lom J, Arthur JR (1989) A guideline for the preparation of species description in Myxosporea. J Fish Dis 12:151–156

    Google Scholar 

  • Lom J, Dyková I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 53:1–36. https://doi.org/10.14411/fp.2006.001

    Article  PubMed  Google Scholar 

  • Mansour L, Al-Qahtani HA, Al-Quraishy S, Abdel-Baki AA (2015) Molecular and morphometric characteristics of Ceratomyxa hamour n. sp. (Myxosporea: Bivalvulida) infecting the gallbladder of the orange-spotted grouper Epinephelus coioides from the Arabian Gulf, Saudi Arabia. J Eukaryot Microbiol 62(1):95–101

    PubMed  Google Scholar 

  • Marino GE, Azzurro A, Massari MG, Finoia AM (2001) Reproduction in the dusky grouper from the southern Mediterranean. J Fish Biol 58:909–927

    Google Scholar 

  • Ottolenghi F, Silvestri C, Giordano P, Lovatelli A, New MB (2004) The fattening of eels, groupers, tunas and yellowtails. In: Captured-based Aquaculture. FAO, Rome

    Google Scholar 

  • Pierre P, Gaillard S, PréVot-D’alvise N, Aubert J, Rostaing-Capaillpn O, Leung-Tack D, Grillasca JP (2008) Grouper aquaculture: Asian success and Mediterranean trials. Aquat Conserv 18:297–308

    Google Scholar 

  • Randall JE (1995) Coastal fishes of Oman. University of Hawaii Press, Honolulu

    Google Scholar 

  • Randall JE, Heemstra PC (1991) Revision of indo-Pacific groupers (Perciformes: Serranidae: Epinephelinae), with descriptions of five new species. Bernice Pauahi Bishop Museum, Honolulu

    Google Scholar 

  • Rangel LF, Cech G, Székely C, Santos MJ (2011) A new actinospore type Unicapsulactinomyxon (Myxozoa), infecting the marine polychaete, Diopatra neapolitana (Polychaeta: Onuphidae) in the Aveiro Estuary (Portugal). Parasitol 138(6):698–712

    CAS  Google Scholar 

  • Rangel LF, Santos MJ, Cech G, Székely C (2009) Morphology, molecular data, and development of Zschokkella mugilis (Myxosporea, Bivalvulida) in a polychaete alternate host, Nereis diversicolor. J Parasitol 95:561–569

    CAS  PubMed  Google Scholar 

  • Reed CC, Basson L, Van As LL, Dyková I (2007) Four new myxozoans (Myxosporea: Bivalvulida) from intertidal fishes along the south coast of Africa. Folia Parasitol 54(4):283–292

    PubMed  Google Scholar 

  • Reñones O, Polunin NVC, Gonῆi R (2002) Size related dietary shifts of Epinephelus marginatus in a western Mediterranean littoral ecosystem: an isotope and stomach content analysis. J Fish Biol 61:122–137

    Google Scholar 

  • Rico MR, Acha M (2003) Southermost occurrence of Epinephelus marginatus in the south-west Atlantic. J Fish Biol 63:1621–1624

    Google Scholar 

  • Rocha S, Casal G, Rangel L, Castro R, Severino R, Azevedo C, Santos MJ (2015) Ultrastructure and phylogeny of Ceratomyxa auratae n. sp. (Myxosporea: Ceratomyxidae), a parasite infecting the gilthead sea bream Sparus aurata (Teleostei: Sparidae). Parasitol Int 64:305–313

    CAS  PubMed  Google Scholar 

  • Rocha S, Rangel LF, Castro R, Severino R, Azevedo C, Santos MJ, Casal G (2016) Ultrastructure and phylogeny of Ceratomyxa diplodae (Myxosporea: Ceratomyxidae), from gall bladder of European seabass Dicentrarchus labrax. Dis Aquat Org 121:117–128

    CAS  PubMed  Google Scholar 

  • Sadovy de Mitcheson Y, Craig MT, Bertoncini AA et al (2013) Fishing groupers towards extinction: a global assessment of threats and extinction risks in a billion dollar fishery. Fish Fish 14(2):119–136

    Google Scholar 

  • Siau Y, Sakiti N (1981) Genre Ceratomyxa (myxosporidies) chez des serranides (poissons, teleosteens). Arch Inst Pasteur Tunis 53(4–3):431–439

    Google Scholar 

  • Thompson JD, Higgins DG, Gilson TJ, Clustal W (1994) Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tortonese E (1986) Serranidae. In: Whitehead PJP, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (eds) Fishes of the north- eastern Atlantic and the Mediterranean, vol II. UNESCO, Paris, pp 780–792

    Google Scholar 

  • Whipps CM, Adlard RD, Bryant MS, Lester RJG, Findlav V, Kent ML (2003) First report of three Kudoa species from eastern Australia: Kudoa thyrsites from Mahi mahi (Coryphaena hippurus), Kudoa amamiensis and Kudoa minithyrsites n. sp. from sweeper (Pempheris ypsilychnus). J Eukaryot Microbiol 50:215–219. https://doi.org/10.1111/j.1550-7408.2003.tb00120.x

    Article  PubMed  Google Scholar 

  • Yokoyama H, Fukuda Y (2001) Ceratomyxa seriolae n. sp. and C. buri n. sp. (Myxozoa: Myxosporea) from the gall-bladder of cultured yellow tail Seriola quinqueradiata. Syst Parasitol 48:125–130

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work is a part of the PhD thesis of Khouloud Bouderbala supported by the University of Tunis El Manar and in part by the Portuguese Strategic Founding Program UID/Multi/04423/2019 to CIIMAR (Interdisciplinary Centre of Marine and Environmental Research).

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Authors and Affiliations

  1. Laboratory of Biodiversity, Parasitology and Ecology of Aquatic Ecosystems, Faculty of Sciences of Tunis, University of Tunis El Manar, 2092, Tunis, Tunisia

    Khouloud Bouderbala & Sihem Bahri

  2. Laboratory of Animal Pathology, Biology Department, Faculty of Sciences (FCUP), University of Porto, Porto, Portugal

    Luis F. Rangel & Maria J. Santos

  3. Interdisciplinary Centre of Marine and Environmental Research (CIIMAR/CIMAR), University of Porto, Porto, Portugal

    Luis F. Rangel & Maria J. Santos

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  1. Khouloud Bouderbala
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  2. Luis F. Rangel
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Correspondence to Khouloud Bouderbala.

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Bouderbala, K., Rangel, L.F., Santos, M.J. et al. Ceratomyxa mennani n. sp. (Myxosporea: Bivalvulida) parasitizing the gallbladder of the dusky grouper Epinephelus marginatus (Serranidae) from Tunisian waters. Parasitol Res 119, 1515–1522 (2020). https://doi.org/10.1007/s00436-020-06649-9

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